Review article: dietary fibre-microbiota interactions

Abstract

Background: Application of modern rapid DNA sequencing technology has transformed our understanding of the gut microbiota. Diet, in particular plant-based fibre, appears critical in influencing the composition and metabolic activity of the microbiome, determining levels of short-chain fatty acids (SCFAs) important for intestinal health.

Aim: To assess current epidemiological, experimental and clinical evidence of how long-term and short-term alterations in dietary fibre intake impact on the microbiome and metabolome.

Methods: A Medline search including items 'intestinal microbiota', 'nutrition', 'diet', 'dietary fibre', 'SCFAs' and 'prebiotic effect' was performed.

Results: Studies found evidence of fibre-influenced differences in the microbiome and metabolome as a consequence of habitual diet, and of long-term or short-term intervention (in both animals and humans).

Conclusions: Agrarian diets high in fruit/legume fibre are associated with greater microbial diversity and a predominance of Prevotella over Bacteroides. 'Western'-style diets, high in fat/sugar, low in fibre, decrease beneficial Firmicutes that metabolise dietary plant-derived polysaccharides to SCFAs and increase mucosa-associated Proteobacteria (including enteric pathogens). Short-term diets can also have major effects, particularly those exclusively animal-based, and those high-protein, low-fermentable carbohydrate/fibre 'weight-loss' diets, increasing the abundance of Bacteroides and lowering Firmicutes, with long-term adherence to such diets likely increasing risk of colonic disease. Interventions to prevent intestinal inflammation may be achieved with fermentable prebiotic fibres that enhance beneficial Bifidobacteria or with soluble fibres that block bacterial-epithelial adherence (contrabiotics). These mechanisms may explain many of the differences in microbiota associated with long-term ingestion of a diet rich in fruit and vegetable fibre.

Figure 1

A plant‐based agrarian diet significantly impacts on the diversity of the intestinal microbiota, which subsequently influences the metabolome. 16S rRNA gene analysis reveal a clear separation of bacterial genera present (>3%) in faecal samples of (a) African (Burkino Faso, BF) and (b) European (EU) children. Pie charts are median values. Outer rings represent corresponding phylum (Bacteroidetes, in green; Firmicutes, in red) for each of the most frequently represented genera. (c) SCFAs are higher in faecal samples from BF vs. EU populations as assessed by SPME‐GC‐MS. (d) Principal Enterobacteriaceae (potentially pathogenic intestinal bacteria) identified are lower in abundance in the microbiota of BF children consuming a diet rich in fruit and legume fibre. Mean (±S.E.M.) are plotted. Significant differences, *P < 0.05; **P ≤ 0.01; ***P ≤ 0.001 (one‐tailed Student's t‐test of all data points). De Filippo et al. 2010; Proc Natl Acad Sci USA 2010; 107(33):14691–6.33 Reproduced with permission.

Figure 2

Short‐term dietary intervention alters the human gut microbiota and microbial activity. Ten subjects were tracked across each diet arm. (a) Fibre intake on the plant‐based diet (rich in grains, legumes, fruits and vegetables) increased (P = 0.007; two‐sided Wilcoxon signed‐rank test) but was negligible on the animal‐based diet (meats, eggs and cheeses). (b) Daily fat intake doubled on the animal‐based diet (P = 0.005), but decreased on the plant‐based diet (P = 0.02). (c) Protein intake also rose on the animal‐based diet (P = 0.005), and decreased on the plant‐based diet (P = 0.005). (d) Microbial diversity within each subject at a given time point (α diversity) did not significantly change during either diet. (e) However, the similarity of each individual's gut microbiota to their baseline communities (β diversity) decreased on the animal‐based diet (dates with q < 0.05 identified with asterisks; Bonferroni‐corrected, two‐sided Mann–Whitney U). Community differences were apparent 1 day after a tracing dye showed the animal‐based diet reached the gut (blue arrows depict appearance of food dyes added to first and last diet day meals). (f) The plant‐based diet generated higher levels of short‐chain fatty acid (SCFAs) typical of plant fibre polysaccharide fermentation than that of the animal‐based diet. (g) Products of dissimilatory amino acid metabolism (branched‐chain SCFAs) by colonic microbiota were seen on the animal‐based diet (*P < 0.05, two‐sided Mann–Whitney U; n = 9–11 faecal samples per diet arm).59 Reproduced with permission from Macmillan Publishers Ltd: Nature, copyright 2014.

Figure 3

Prebiotic intervention with arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiome and metabolome of humanised rats. (a) The intestinal microbiota at the site of fermentation (caecum) in humanised rats fed a diet supplemented with long‐chain arabinoxylan (LC‐AX) or inulin (IN) is significantly different to those fed control diet (P = 0.002). The redundancy analysis (RDA) at bacterial group‐level is based on the human intestinal tract (HIT) Chip microarray data performed on samples from final day of intervention (n = 4). Of 131 bacterial groups identified with HITC hip, 22 groups were retained (average cumulative abundance of these 22 groups = 42%) explaining 31.9% of the variation between these diets along the x‐axis and 16.3% of the variation along the y‐axis. (b) Absolute levels of SCFA (total and individual; μmol/g wet caecal content) at the end of the intervention were increased in the caecum of humanised rats fed LC‐AX or IN (n = 8), whereas ammonium levels (indicative of protein metabolism) decreased. Values indicated with a different superscript are significantly different (a, b or c).83 Reproduced from Van den Abbeele et al. Environmental Microbiology 2011; 13(10): 2667–80. with permission of Wiley.com.

Figure 4

Contrabiotic plantain (banana) NSP blocks translocation of Crohn's disease mucosa‐associated Escherichia coli across the human intestinal epithelium. Histology of (a) human villus epithelium (VE) and of (b) an ileal lymphoid follicle (LF) and overlying follicle‐associated epithelium (FAE) following Ussing chamber experiments (×20 magnification). (c, d) Colonic Crohn's E. coli isolate HM615 translocation across ileal FAE (N = 7) and VE (N = 9) is inhibited by 20 min pre‐treatment with plantain NSP. **P < 0.01; ***P < 0.001; anova. (e) Overnight culture of Ussing chamber serosal medium following 2‐h translocation of Crohn's disease E. coli HM 615 across isolated human epithelium, in the presence and absence of plantain NSP. Reproduced from Roberts et al. Gut 2010; 59(10):1331–9, with permission from BMJ Publishing Group Ltd.119

Figure 5

Overview of the long‐term and short‐term impact of dietary fibre on the intestinal microbiome and metabolome. An agrarian diet increases faecal microbial diversity (increased Firmicutes, reduced Proteobacteria) and encourages growth of bacteria that produce short‐chain fatty acids (such as butyrate, acetate and proprionate) ‐ all considered to be “good” for gut health. Western diet and high protein/low fermentable carbohydrate/fibre diets induce largely opposite changes which are theoretically “bad” for gut health. AA, aminoacid; AIEC, adherent, invasive E. coli; CHO, carbohydrate; FODMAP, fermentable oligo‐, di‐ and monosaccharides and polyols; SCFA, short‐chain fatty acids; spp., species.